Breeders often
talk about inbreeding and outcrossing as though they were the only
possibilities -- and generally with negative comments about the
latter. There are other possibilities, and I have long been a
proponent of assortative mating. It is not a theoretical concept that
doesn't work in practice; I know several breeders who do it and
achieve good results. This essay will attempt to explain why it is a
good idea, but first I need to define the alternatives.

Random Mating

Though random
mating is not a common breeding practice, understanding what this
implies is important. Random mating is exactly what the name implies:
mates are chosen with no regard for similarity or relatedness. (If
the population is inbred to some extent, randomly-selected mates may
be related.)

Random mating is
one of the assumptions behind the Hardy-Weinberg formula, which
allows one to calculate the frequency of heterozygous carriers from
the frequency of individuals expressing some recessive trait in a
population. Because inbreeding among purebred dogs and in other small
populations decreases the frequency of heterozygotes, these estimates
may be higher than the actual incidence.

Inbreeding and Linebreeding

Inbreeding is the
practice of breeding two animals that are related (i.e., have one or
more common ancestors). The degree of inbreeding may be assigned a
value between 0 and 1, called the inbreeding coefficient, where 0
indicates that the animals have no common ancestors. Because the
number of ancestors potentially doubles with every generation you go
back in a pedigree, you eventually get to a point, even in a very
large population, where there are simply not enough ancestors. Thus,
all populations are inbred to some degree, and a true outcross (the
term generally used when two animals are "unrelated") is
not really possible. The term is generally misused to describe a
cross between two animals with different phenotypes.

In a population
with a limited number of founders, a maximum number of ancestors --
the effective population size -- is reached in some past generation.
This number will be governed by various factors, such as the total
population size, how far individuals travel during their lifetime,
and whether there are inbreeding taboos or other mechanisms that
reduce the likelihood of close relatives mating.

Inbreeding does
not change allele frequencies directly, but it does increase the
proportion of homozygotes. Individuals homozygous for deleterious
genes are likely to be removed from the breeding pool by natural
selection (if they do not survive to reproductive age) or by man.

Linebreeding is
merely a term used for a particular type of inbreeding that often
focusses on one ancestor who was considered exceptional. Particularly
if it is a male, this exceptional ancestor may end up as grandfather
and great-grandfather -- sometimes more than once -- in the same
pedigree. Father-daughter, mother-son, and some other combinations
also result in a disproportionate number of genes coming from a
single ancestor. This type of close inbreeding is less common. [In
contrast, the mating of full sibs or first cousins doubles up on two
ancestors equally.]

As the result of
several common practices, most pure-bred domestic animals are more
inbred than they really need to be. One is that some breeders own a
small number of animals and breed only within their own group. A
second is that many breeders have the idea that outstanding animals
can be produced by inbreeding -- by doubling up on the good alleles
while somehow avoiding the bad. Even if you were to point out that
this is a gamble, such breeders might respond that they are simply
helping natural selection.

Beyond the
conventional close-relative inbreeding, there is another practice
that has much the same effect, namely the popular sire phenomenon
(generally over-use of a well-promoted champion). In fact, many who
breed to such a dog believe they are doing a "good thing,"
as they will be increasing the frequency of occurrence of the genes
that made him a champion. What they may not realize is that they are
increasing the frequency of all genes carried by this animal --
whether they are good, bad, or innocuous -- and that champions, like
any other animal, carry a number of undesirable recessive alleles
(the genetic load) that are masked by wild-type alleles. The result
of the popular sire phenomenon is that almost all members of the
breed will carry a little bit of Jake Hugelberg, and any undesirable
trait carried by Jake will no longer be rare. Finding a safe,
unrelated mate then becomes an exercise in futility.

If we lived in a
world where all the genes followed the simple rule that there may
only be good alleles, which are dominant, and bad alleles, which are
recessive, then inbreeding could be an effective tool for improving a
breed. However, during the past 25 years, geneticists have been
directly measuring genetic diversity in populations by looking at the
DNA or proteins, rather than at the phenotype. They have found that
many individuals who cannot easily be distinguished by their
phenotypic appearance nevertheless have considerable differences in
their genotype. Some of these alternative alleles (termed neutral
isoalleles) are functionally equivalent. Others have lost only a
small portion of their normal function.

Suppose we have a
"mutant" allele that has lost only 5-10% of its normal
function. In many cases, this would not produce a noticeable effect.
If you made an individual homozygous for this allele, you would not
even be aware that you had done so. Now consider that the same fate
may befall a number of genes during an inbreeding program.
Eventually, you will have an individual that is considerably less fit
than one carrying the normal alleles for all (or even most of) these
genes. There is no magic formula for regaining what you have lost.
You must start again.

[Sometimes mutant
alleles result in an even more dramatic loss of function, but remain
undiscovered under normal conditions. A good example is vWD in Dobermans.]

About the only
animals that are routinely inbred to a high level are laboratory mice
and rats. There, the breeders start breeding many lines
simultaneously in the expectation that the majority will die out or
will suffer significant inbreeding depression, which generally means
that they are smaller, produce fewer offspring, are more susceptible
to disease, and have a shorter average lifespan. Dogs are no
different. If you can start with enough lines, a few may make it
through the genetic bottleneck with acceptable fitness. However, dog
breeders generally don't have the resources to start several dozen or
more lines simultaneously.

Sometimes two
different alleles may be better than one. Consider the major
histocompatibility complex (MHC). These genes are responsible for
distinguishing "self" from "foreign", and a
heterozygous individual can recognize more possibilities than a
homozygous one. Having a variety of MHC alleles is even more
important to population survival. Not only does this provide better
defense against pathogens, but there is growing evidence that parents
who carry different MHC haplotypes may have fewer fertility problems.
This is not a universally accepted theory, but today one is hard
pressed to find a conservation or zoo biologist concerned with
preserving an endangered species who would not list maintaining
maximum genetic diversity as one of his/her primary goals.

Assortative Mating

Assortative mating
is the mating of individuals that are phenotypically similar. It is a
normal practice, to some degree, for humans and various other
species. Though phenotype is a product of both genotype and
environment, such individuals are more likely to carry the same
alleles for genes determining morphology. If we are talking about a
conformation that is basically sound from the structural point of
view, the genes involved will have been subjected to natural
selection for thousands of years and will most likely be dominant.
The major characteristics that set one breed apart from another will
likely have been fixed early in the breed's history.
("Fixed" means that there is only one allele of present in
the population. If there is only one allele, the question of
dominance does not arise.) Consequently, when you look at a dog, you
are looking at his genes. If the conformation (or, for that matter,
the temperament, intelligence, or whatever) is not good, then you are
very likely looking at a dog or a breed that is homozygous for one or
more recessive alleles that you would probably like to get rid of. If
it is the dog and not the breed, you may elect not to breed him, or
you may look for a mate that covers the problem. If it is the breed,
the only solution would be to introduce some genes from another
breed. (That would be an outcross!)

Breeding together
animals that share dominant good alleles for most of their genes will
produce mainly puppies that also carry these genes. Even if the
parents are not homozygous for all these good alleles, you should
still get many that are suitable. More important, if animals
heterozygous for certain genes are more fit, assortative mating will
preserve more heterozygosity than inbreeding. However, unlike
inbreeding, assortative mating should not result in an increased risk
of the parents sharing hidden recessive mutations. Though we might
like to eliminate deleterious recessives, everyone carries a few.
Trying to find the "perfect dog" without either visible or
hidden flaws is like betting on the lottery. There may conceivably be
a big winner out there, but they are certainly not common.

The more you try
to cover the deficiencies in one dog with good qualities in another,
the less the dogs will have in common. If, then, the results are
unsatisfactory, they should not be blamed on assortative mating, as
that is no longer what you are doing.

The risks involved

Some trait that
breeders consider desirable could be the result of homozygosity for a
recessive allele for gene A or gene B. Obviously, crossing an AAbb
with an aaBB will produce AaBb progeny that will not express this
trait. (However, aside from some of the genes affecting coat color, I
can think of no examples.)

If care is not
taken to go back far enough in the pedigrees, you may have two
animals with similar phenotypes resulting from common ancestry.
Whether you are inbreeding unintentionally or intentionally, the
consequences are the same. The solution is simple: check the heritage.

Because
assortative mating involves selection (you are hopefully mating the
best together, and not the worst), you are denying some dogs the
opportunity to pass their genes on to the next generation. This is,
perhaps, the subtlest of risks, as it does not seem to involve doing
anything "wrong." Most would argue that it is merely doing
what nature does -- eliminating the least fit. But what if some of
these "less-than-best" happen to be the only ones to carry
the best allele for some gene? Out goes the good with the bad!

This is primarily
a "low-numbers" risk. The larger the population, the less
likely we are to find that important alleles are carried by only a
few individuals. However, it pays to know where the diversity lies.
Do any of you know which, among the current dogs, are most likely to
carry the genes of any given founder?

Notes

Inbreeding
calculations do not account for the possibility that an allele will
become homozygous by "chance," though this, too, can be
calculated if the frequency at which an allele occurs in the whole
population is known. Most basic Genetics texts explain how. (See, for
example, Willis, pp. 293-295, "The Hardy-Weinberg Law.")

I have seen
figures of 2500 genetic diseases in man and there are likely to be as
many in Canis familiaris, taken as a whole. In man. the vast majority
are rare (allele frequencies of < 0.01, which means < 1 in 1000
affected). However, everyone carries three to five "lethal
equivalents." This is their "genetic load." Canine
breeds are often established with a handful of founders, so we end up
with a subset of one or two dozen problems, at frequencies at least
10-fold higher. [If we had five founders, each with a unique set of
problems carried as single recessive alleles, the allele frequency of
each will initially be ~ 0.1 and ~ 1% will be affected.